Irritable bowel syndrome: Methods, mechanisms, and pathophysiology. Methods to assess visceral hypersensitivity in irritable bowel syndrome

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 303, Issue 2, 2012, Pages

  Keszthelyi, D ^a,b   Troost, F J ^a,b   Masclee, A A ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Brain imaging; Rectal distension; Visceral nociception

Indexed keywords

CORTICOTROPIN RELEASING FACTOR ANTAGONIST; NEUROKININ 1 RECEPTOR ANTAGONIST;

ARTICLE; AUTONOMIC DYSFUNCTION; COLON DILATATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INNERVATION; IRRITABLE COLON; MAGNETOENCEPHALOGRAPHY; NEUROIMAGING; NEUROPHYSIOLOGY; NOCICEPTION; PAIN ASSESSMENT; PATHOPHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SPINAL CORD; SPINAL REFLEX; VISCERAL PAIN;

ABDOMINAL PAIN; ANIMALS; AUTONOMIC NERVOUS SYSTEM; FEMALE; HUMANS; IRRITABLE BOWEL SYNDROME; MALE; MICE; NEUROIMAGING; NOCICEPTION; PAIN MEASUREMENT; RATS; VISCERAL PAIN;

EID: 84863884642     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00060.2012     Document Type: Article

References (120)

1. Accarino AM, Azpiroz F, Malagelada JR. Symptomatic responses to stimulation of sensory pathways in the jejunum. Am J Physiol Gastrointest Liver Physiol 263: G673-G677, 1992.
2. Al-Chaer ED, Traub RJ. Biological basis of visceral pain: recent developments. Pain 96: 221-225, 2002.
3. Ammons WS, Girardot MN, Foreman RD. T2-T5 spinothalamic neurons projecting to medial thalamus with viscerosomatic input. J Neurophysiol 54: 73-89, 1985.
4. Anand P, Aziz Q, Willert R, van Oudenhove L. Peripheral and central mechanisms of visceral sensitization in man. Neurogastroenterol Motil 19: 29-46, 2007.
5. Andrews PL, Sanger GJ. Abdominal vagal afferent neurones: an important target for the treatment of gastrointestinal dysfunction. Curr Opin Pharmacol 2: 650-656, 2002.
6. Arebi N, Bullas DC, Dukes GE, Gurmany S, Hicks KJ, Kamm MA, Hobson AR. Distinct neurophysiological profiles in irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 300: G1086-G1093, 2011.
7. Azpiroz F, Bouin M, Camilleri M, Mayer EA, Poitras P, Serra J, Spiller RC. Mechanisms of hypersensitivity in IBS and functional disorders. Neurogastroenterol Motil 19: 62-88, 2007.
8. Basbaum AI, Fields HL. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7: 309-338, 1984.
9. Bearcroft CP, Perrett D, Farthing MJ. Postprandial plasma 5-hydroxytryptamine in diarrhoea predominant irritable bowel syndrome: a pilot study. Gut 42: 42-46, 1998.
10. Berman SM, Chang L, Suyenobu B, Derbyshire SW, Stains J, Fitzgerald L, Mandelkern M, Hamm L, Vogt B, Naliboff BD, Mayer EA. Condition-specific deactivation of brain regions by 5-HT3 receptor antagonist Alosetron. Gastroenterology 123: 969-977, 2002.
11. Berman SM, Naliboff BD, Suyenobu B, Labus JS, Stains J, Ohning G, Kilpatrick L, Bueller JA, Ruby K, Jarcho J, Mayer EA. Reduced brainstem inhibition during anticipated pelvic visceral pain correlates with enhanced brain response to the visceral stimulus in women with irritable bowel syndrome. J Neurosci 28: 349-359, 2008.
12. Bingel U, Lorenz J, Schoell E, Weiller C, Buchel C. Mechanisms of placebo analgesia: rACC recruitment of a subcortical antinociceptive network. Pain 120: 8-15, 2006.
13. Blackshaw LA, Gebhart GF. The pharmacology of gastrointestinal nociceptive pathways. Curr Opin Pharmacol 2: 642-649, 2002.
14. Bouhassira D, Sabate JM, Coffin B, Le Bars D, Willer JC, Jian R. Effects of rectal distensions on nociceptive flexion reflexes in humans. Am J Physiol Gastrointest Liver Physiol 275: G410-G417, 1998.
15. Bouin M, Plourde V, Boivin M, Riberdy M, Lupien F, Laganiere M, Verrier P, Poitras P. Rectal distention testing in patients with irritable bowel syndrome: sensitivity, specificity, and predictive values of pain sensory thresholds. Gastroenterology 122: 1771-1777, 2002.
16. Bradette M, Delvaux M, Staumont G, Fioramonti J, Bueno L, Frexinos J. Octreotide increases thresholds of colonic visceral perception in IBS patients without modifying muscle tone. Dig Dis Sci 39: 1171-1178, 1994.
17. Brierley SM, Carter R, Jones W 3rd, Xu L, Robinson DR, Hicks GA, Gebhart GF, Blackshaw LA. Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J Physiol 567: 267-281, 2005.
18. Brierley SM, Jones RC 3rd, Gebhart GF, Blackshaw LA. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 127: 166-178, 2004.
19. Brierley SM, Jones RC 3rd, Xu L, Gebhart GF, Blackshaw LA. Activation of splanchnic and pelvic colonic afferents by bradykinin in mice. Neurogastroenterol Motil 17: 854-862, 2005.
20. Bromm B, Scharein E, Vahle-Hinz C. Cortex areas involved in the processing of normal and altered pain. Prog Brain Res 129: 289-302, 2000.
21. Caldarella MP, Milano A, Laterza F, Sacco F, Balatsinou C, Lapenna D, Pierdomenico SD, Cuccurullo F, Neri M. Visceral sensitivity and symptoms in patients with constipation-or diarrhea-predominant irritable bowel syndrome (IBS): effect of a low-fat intraduodenal infusion. Am J Gastroenterol 100: 383-389, 2005.
22. Camilleri M. Testing the sensitivity hypothesis in practice: tools and methods, assumptions and pitfalls. Gut 51, Suppl 1: i34-i40, 2002.
23. Casey KL. Reticular formation and pain: toward a unifying concept. Res Publ Assoc Res Nerv Ment Dis 58: 93-105, 1980.
24. Chan YK, Herkes GK, Badcock C, Evans PR, Bennett E, Kellow JE. Alterations in cerebral potentials evoked by rectal distension in irritable bowel syndrome. Am J Gastroenterol 96: 2413-2417, 2001.
25. Chey WD, Beydoun A, Roberts DJ, Hasler WL, Owyang C. Octreotide reduces perception of rectal electrical stimulation by spinal afferent pathway inhibition. Am J Physiol Gastrointest Liver Physiol 269: G821-G826, 1995.
26. Chung JM, Lee KH, Surmeier DJ, Sorkin LS, Kim J, Willis WD. Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. J Neurophysiol 56: 370-390, 1986.
27. Coen SJ, Gregory LJ, Yaguez L, Amaro E Jr, Brammer M, Williams SC, Aziz Q. Reproducibility of human brain activity evoked by esophageal stimulation using functional magnetic resonance imaging. Am J Physiol Gastrointest Liver Physiol 293: G188-G197, 2007.
28. Coffin B, Bouhassira D, Sabate JM, Barbe L, Jian R. Alteration of the spinal modulation of nociceptive processing in patients with irritable bowel syndrome. Gut 53: 1465-1470, 2004.
29. Coffin B, Farmachidi JP, RuEEGg P, Bastie A, Bouhassira D. Tegaserod, a 5-HT4 receptor partial agonist, decreases sensitivity to rectal distension in healthy subjects. Aliment Pharmacol Ther 17: 577-585, 2003.
30. Collet L, Meunier P, Duclaux R, Chery-Croze S, Falipou P. Cerebral evoked potentials after endorectal mechanical stimulation in humans. Am J Physiol Gastrointest Liver Physiol 254: G477-G482, 1988.
31. Cremonini F, Houghton LA, Camilleri M, Ferber I, Fell C, Cox V, Castillo EJ, Alpers DH, Dewit OE, Gray E, Lea R, Zinsmeister AR, Whorwell PJ. Barostat testing of rectal sensation and compliance in humans: comparison of results across two centres and overall reproducibility. Neurogastroenterol Motil 17: 810-820, 2005.
32. De Broucker T, Cesaro P, Willer JC, Le Bars D. Diffuse noxious inhibitory controls in man. Involvement of the spinoreticular tract. Brain 113: 1223-1234, 1990.
33. Delvaux M. Do we need to perform rectal distention tests to diagnose IBS in clinical practice? Gastroenterology 122: 2075-2078, 2002.
34. Delvaux M, Louvel D, Lagier E, Scherrer B, Abitbol JL, Frexinos J. The kappa agonist fedotozine relieves hypersensitivity to colonic distention in patients with irritable bowel syndrome. Gastroenterology 116: 38-45, 1999.
35. Derbyshire SW. A systematic review of neuroimaging data during visceral stimulation. Am J Gastroenterol 98: 12-20, 2003.
36. Dorn SD, Palsson OS, Thiwan SI, Kanazawa M, Clark WC, van Tilburg MA, Drossman DA, Scarlett Y, Levy RL, Ringel Y, Crowell MD, Olden KW, Whitehead WE. Increased colonic pain sensitivity in irritable bowel syndrome is the result of an increased tendency to report pain rather than increased neurosensory sensitivity. Gut 56: 1202-1209, 2007.
37. Drewes AM, Petersen P, Rossel P, Gao C, Hansen JB, Arendt-Nielsen L. Sensitivity and distensibility of the rectum and sigmoid colon in patients with irritable bowel syndrome. Scand J Gastroenterol 36: 827-832, 2001.
38. Drossman DA, Camilleri M, Mayer EA, Whitehead WE. AGA technical review on irritable bowel syndrome. Gastroenterology 123: 2108-2131, 2002.
39. Feng B, Brumovsky PR, Gebhart GF. Differential roles of stretchsensitive pelvic nerve afferents innervating mouse distal colon and rectum. Am J Physiol Gastrointest Liver Physiol 298: G402-G409, 2010.
40. Feng B, Gebhart GF. Characterization of silent afferents in the pelvic and splanchnic innervations of the mouse colorectum. Am J Physiol Gastrointest Liver Physiol 300: G170-G180, 2011.
41. Feng B, La JH, Schwartz ES, Tanaka T, McMurray TP, Gebhart GF. Long-term sensitization of mechanosensitive and-insensitive afferents in mice with persistent colorectal hypersensitivity. Am J Physiol Gastrointest Liver Physiol 302: G676-G683, 2012.
42. Fuhrer M, Vogelsang H, Hammer J. A placebo-controlled trial of an oral capsaicin load in patients with functional dyspepsia. Neurogastroenterol Motil 23: 918-e397, 2011.
43. Gebhart GF. Descending modulation of pain. Neurosci Biobehav Rev 27: 729-837, 2004.
44. Gold M. Overview of pain and sensitization. In: Chronic Abdominal and Visceral Pain, edited by Pasricha PJ, Willis WD, Gebhart GF. New York: Informa Healthcare, 2007, p. 17-32.
45. Hammer HF, Phillips SF, Camilleri M, Hanson RB. Rectal tone, distensibility, and perception: reproducibility and response to different distensions. Am J Physiol Gastrointest Liver Physiol 274: G584-G590, 1998.
46. Hammer J, Hammer HF, Eherer AJ, Petritsch W, Holzer P, Krejs GJ. Intraluminal capsaicin does not affect fluid and electrolyte absorption in the human jejunum but does cause pain. Gut 43: 252-255, 1998.
47. Harris ML, Hobson AR, Hamdy S, Thompson DG, Akkermans LM, Aziz Q. Neurophysiological evaluation of healthy human anorectal sensation. Am J Physiol Gastrointest Liver Physiol 291: G950-G958, 2006.
48. Heiss WD, Herholz K. Brain receptor imaging. J Nucl Med 47: 302-312, 2006.
49. Hobson AR, Aziz Q. Brain imaging and functional gastrointestinal disorders: has it helped our understanding? Gut 53: 1198-1206, 2004.
50. Hobson AR, Furlong PL, Sarkar S, Matthews PJ, Willert RP, Worthen SF, Unsworth BJ, Aziz Q. Neurophysiologic assessment of esophageal sensory processing in noncardiac chest pain. Gastroenterology 130: 80-88, 2006.
51. Hobson AR, Sarkar S, Furlong PL, Thompson DG, Aziz Q. A cortical evoked potential study of afferents mediating human esophageal sensation. Am J Physiol Gastrointest Liver Physiol 279: G139-G147, 2000.
52. Hubbard CS, Labus JS, Bueller J, Stains J, Suyenobu B, Dukes GE, Kelleher DL, Tillisch K, Naliboff BD, Mayer EA. Corticotropinreleasing factor receptor 1 antagonist alters regional activation and effective connectivity in an emotional-arousal circuit during expectation of abdominal pain. J Neurosci 31: 12491-12500, 2011.
53. Hughes PA, Brierley SM, Martin CM, Brookes SJ, Linden DR, Blackshaw LA. Post-inflammatory colonic afferent sensitisation: different subtypes, different pathways and different time courses. Gut 58: 1333-1341, 2009.
54. Hugon M. Exteroceptive reflexes to stimulation of the sural nerve in normal man. In: New Developments in Electromyography and Clinical Neurophysiology, edited by Desmedt JE. Basel: Karger, 1973, p. 713-729.
55. Iovino P, Azpiroz F, Domingo E, Malagelada JR. The sympathetic nervous system modulates perception and reflex responses to gut distention in humans. Gastroenterology 108: 680-686, 1995.
56. Kanazawa M, Palsson OS, Thiwan SI, Turner MJ, van Tilburg MA, Gangarosa LM, Chitkara DK, Fukudo S, Drossman DA, Whitehead WE. Contributions of pain sensitivity and colonic motility to IBS symptom severity and predominant bowel habits. Am J Gastroenterol 103: 2550-2561, 2008.
57. Keszthelyi D, Troost FJ, Simren M, Ludidi S, Kruimel JW, Conchillo JM, Masclee AA. Revisiting concepts of visceral nociception in irritable bowel syndrome. Eur J Pain 2012. doi: 10.1002/j.1532-2149.2012.00147.x. [Epub ahead of print].
58. Kingham JG, Dawson AM. Origin of chronic right upper quadrant pain. Gut 26: 783-788, 1985.
59. Kuiken SD, Lindeboom R, Tytgat GN, Boeckxstaens GE. Relationship between symptoms and hypersensitivity to rectal distension in patients with irritable bowel syndrome. Aliment Pharmacol Ther 22: 157-164, 2005.
60. Kyloh M, Nicholas S, Zagorodnyuk VP, Brookes SJ, Spencer NJ. Identification of the visceral pain pathway activated by noxious colorectal distension in mice. Front Neurosci 5: 16, 2011.
61. Lackner JM, Lou Coad M, Mertz HR, Wack DS, Katz LA, Krasner SS, Firth R, Mahl TC, Lockwood AH. Cognitive therapy for irritable bowel syndrome is associated with reduced limbic activity, GI symptoms, and anxiety. Behav Res Ther 44: 621-638, 2006.
62. Larsson MB, Tillisch K, Craig AD, Engstrom M, Labus J, Naliboff B, Lundberg P, Strom M, Mayer EA, Walter SA. Brain responses to visceral stimuli reflect visceral sensitivity thresholds in patients with irritable bowel syndrome. Gastroenterology 142: 463-472.e3, 2012.
63. Le Bars D, Dickenson AH, Besson JM. Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain 6: 283-304, 1979.
64. Lembo T, Munakata J, Mertz H, Niazi N, Kodner A, Nikas V, Mayer EA. Evidence for the hypersensitivity of lumbar splanchnic afferents in irritable bowel syndrome. Gastroenterology 107: 1686-1696, 1994.
65. Lembo T, Munakata J, Naliboff B, Fullerton S, Mayer EA. Sigmoid afferent mechanisms in patients with irritable bowel syndrome. Dig Dis Sci 42: 1112-1120, 1997.
66. Lembo T, Naliboff BD, Matin K, Munakata J, Parker RA, Gracely RH, Mayer EA. Irritable bowel syndrome patients show altered sensitivity to exogenous opioids. Pain 87: 137-147, 2000.
67. Li Y, Wang Y, Zuo X, Guo Y, Zhang H, Lu X, Li J, Desmond PV. Visceral perception thresholds after rectal thermal and pressure stimuli in irritable bowel syndrome patients. J Gastroenterol Hepatol 19: 187-191, 2004.
68. Loening-Baucke V, Read NW, Yamada T. Cerebral evoked potentials after rectal stimulation. Electroencephalogr Clin Neurophysiol 80: 490-495, 1991.
69. Ludidi S, Conchillo JM, Keszthelyi D, Koning CJ, Vanhoutvin SA, Lindsey PJ, Leufkens AM, Kruimel JW, Jonkers DM, Masclee AA. Does meal ingestion enhance sensitivity of visceroperception assessment in irritable bowel syndrome? Neurogastroenterol Motil 24: 47-53.e3, 2012.
70. Ludidi S, Conchillo JM, Keszthelyi D, Van Avesaat M, Kruimel JW, Jonkers DM, Masclee AA. Rectal hypersensitivity as hallmark for irritable bowel syndrome: defining the optimal cutoff. Neurogastroenterol Motil 2012. doi:10.1111/j.1365-2982.2012.01926.x. [Epub ahead of print].
71. Lynn PA, Blackshaw LA. In vitro recordings of afferent fibres with receptive fields in the serosa, muscle and mucosa of rat colon. J Physiol 518: 271-282, 1999.
72. Mason P. Descending pain modulation as a component of homeostasis. In: Handbook of Clinical Neurology Pain, edited by Cervero F, Jensen TS. London: Elsevier; 2006, vol. 81, p. 211-220.
73. Mayer EA. Spinal and supraspinal modulation of visceral sensation. Gut 47, Suppl 4: iv69-iv72; discussion iv6, 2000.
74. Mayer EA, Bradesi S, Chang L, Spiegel BM, Bueller JA, Naliboff BD. Functional GI disorders: from animal models to drug development. Gut 57: 384-404, 2008.
75. Mazurak N, Seredyuk N, Sauer H, Teufel M, Enck P. Heart rate variability in the irritable bowel syndrome: a review of the literature. Neurogastroenterol Motil 24: 206-216, 2012.
76. Mertz H, Naliboff B, Munakata J, Niazi N, Mayer EA. Altered rectal perception is a biological marker of patients with irritable bowel syndrome. Gastroenterology 109: 40-52, 1995.
77. Micalos PS, Drinkwater EJ, Cannon J, Arendt-Nielsen L, Marino FE. Reliability of the nociceptive flexor reflex (RIII) threshold and association with Pain threshold. Eur J Appl Physiol 105: 55-62, 2009.
78. Morgan V, Pickens D, Gautam S, Kessler R, Mertz H. Amitriptyline reduces rectal pain related activation of the anterior cingulate cortex in patients with irritable bowel syndrome. Gut 54: 601-607, 2005.
79. Naliboff BD, Berman S, Suyenobu B, Labus JS, Chang L, Stains J, Mandelkern MA, Mayer EA. Longitudinal change in perceptual and brain activation response to visceral stimuli in irritable bowel syndrome patients. Gastroenterology 131: 352-365, 2006.
80. Naliboff BD, Mayer EA. Brain imaging in IBS: drawing the line between cognitive and non-cognitive processes. Gastroenterology 130: 267-270, 2006.
81. Ness TJ, Gebhart GF. Visceral pain: a review of experimental studies. Pain 41: 167-234, 1990.
82. Olsson C, Chen BN, Jones S, Chataway TK, Costa M, Brookes SJ. Comparison of extrinsic efferent innervation of guinea pig distal colon and rectum. J Comp Neurol 496: 787-801, 2006.
83. Pessoa L. On the relationship between emotion and cognition. Nat Rev Neurosci 9: 148-158, 2008.
84. Piche M, Arsenault M, Poitras P, Rainville P, Bouin M. Widespread hypersensitivity is related to altered pain inhibition processes in irritable bowel syndrome. Pain 148: 49-58, 2010.
85. Posserud I, Syrous A, Lindstrom L, Tack J, Abrahamsson H, Simren M. Altered rectal perception in irritable bowel syndrome is associated with symptom severity. Gastroenterology 133: 1113-1123, 2007.
86. Price DD. Central neural mechanisms that interrelate sensory and affective dimensions of pain. Mol Interv 2: 392-403, 339, 2002.
87. Price DD, Bush FM, Long S, Harkins SW. A comparison of pain measurement characteristics of mechanical visual analogue and simple numerical rating scales. Pain 56: 217-226, 1994.
88. Price DD, Robinson ME, Verne GN. Measuring pain and hyperalgesia in persistent pain conditions with a special emphasis on irritable bowel syndrome. In: Chronic Abdominal and Visceral Pain, edited by Pasricha PJ, Willis WD, Gebhart GF. New York: Informa Healthcare, 2007, p. 127-140.
89. Ragnarsson G, Bodemar G. Pain is temporally related to eating but not to defaecation in the irritable bowel syndrome (IBS). Patients' description of diarrhea, constipation and symptom variation during a prospective 6-week study. Eur J Gastroenterol Hepatol 10: 415-421, 1998.
90. Ritchie J. Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 14: 125-132, 1973.
91. Rossel P, Drewes AM, Petersen P, Nielsen J, Arendt-Nielsen L. Pain produced by electric stimulation of the rectum in patients with irritable bowel syndrome: further evidence of visceral hyperalgesia. Scand J Gastroenterol 34: 1001-1006, 1999.
92. Sabate JM, Bouhassira D, Poupardin C, Wagner A, Loria Y, Coffin B. Sensory signalling effects of tegaserod in patients with irritable bowel syndrome with constipation. Neurogastroenterol Motil 20: 134-141, 2008.
93. Sabate JM, Gorbatchef C, Flourie B, Jian R, Coffin B. Cholecystokinin octapeptide increases rectal sensitivity to pain in healthy subjects. Neurogastroenterol Motil 14: 689-695, 2002.
94. Sandrini G, Serrao M, Rossi P, Romaniello A, Cruccu G, Willer JC. The lower limb flexion reflex in humans. Prog Neurobiol 77: 353-395, 2005.
95. Sharma A, Aziz Q. Mechanisms of visceral sensitization in humans. In: Chronic Abdominal and Visceral Pain, edited by Pasricha PJ, Willis WD, Gebhart GF. New York: Informa Healthcare, 2007, p. 141-160.
96. Sheehan J, Gaman A, Vangel M, Kuo B. Pooled analysis of brain activity in irritable bowel syndrome and controls during rectal balloon distension. Neurogastroenterol Motil 23: 336-346.e158, 2011.
97. Sherrington CS. Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J Physiol 40: 28-121, 1910.
98. Simren M, Abrahamsson H, Bjornsson ES. An exaggerated sensory component of the gastrocolonic response in patients with irritable bowel syndrome. Gut 48: 20-27, 2001.
99. Simren M, Agerforz P, Bjornsson ES, Abrahamsson H. Nutrientdependent enhancement of rectal sensitivity in irritable bowel syndrome (IBS). Neurogastroenterol Motil 19: 20-29, 2007.
100. Simren M, Mansson A, Langkilde AM, Svedlund J, Abrahamsson H, Bengtsson U, Bjornsson ES. Food-related gastrointestinal symptoms in the irritable bowel syndrome. Digestion 63: 108-115, 2001.
101. Simren M, Simms L, D'Souza D, Abrahamsson H, Bjornsson ES. Lipid-induced colonic hypersensitivity in irritable bowel syndrome: the role of 5-HT3 receptors. Aliment Pharmacol Ther 17: 279-287, 2003.
102. Sinhamahapatra P, Saha SP, Chowdhury A, Chakrabarti SK, Ghosh A, Maiti B. Visceral afferent hypersensitivity in irritable bowel syndrome-evaluation by cerebral evoked potential after rectal stimulation. Am J Gastroenterol 96: 2150-2157, 2001.
103. Smith JK, Humes DJ, Head KE, Bush D, White TP, Stevenson CM, Brookes MJ, Marciani L, Spiller RC, Gowland PA, Francis ST. fMRI and MEG analysis of visceral pain in healthy volunteers. Neurogastroenterol Motil 23: 648.e260, 2011.
104. Spaziani R, Bayati A, Redmond K, Bajaj H, Mazzadi S, Bienenstock J, Collins SM, Kamath MV. Vagal dysfunction in irritable bowel syndrome assessed by rectal distension and baroreceptor sensitivity. Neurogastroenterol Motil 20: 336-342, 2008.
105. Spetalen S, Jacobsen MB, Vatn MH, Blomhoff S, Sandvik L. Visceral sensitivity in irritable bowel syndrome and healthy volunteers: reproducibility of the rectal barostat. Dig Dis Sci 49: 1259-1264, 2004.
106. Sugiura Y, Terui N, Hosoya Y, Tonosaki Y, Nishiyama K, Honda T. Quantitative analysis of central terminal projections of visceral and somatic unmyelinated (C) primary afferent fibers in the guinea pig. J Comp Neurol 332: 315-325, 1993.
107. Tillisch K, Labus J, Nam B, Bueller J, Smith S, Suyenobu B, Siffert J, McKelvy J, Naliboff B, Mayer E. Neurokinin-1-receptor antagonism decreases anxiety and emotional arousal circuit response to noxious visceral distension in women with irritable bowel syndrome: a pilot study. Aliment Pharmacol Ther 35: 360-367, 2012.
108. Tillisch K, Mayer EA, Labus JS. Quantitative meta-analysis identifies brain regions activated during rectal distension in irritable bowel syndrome. Gastroenterology 140: 91-100, 2011.
109. Turner R. Magnetic resonance imaging of brain function. Am J Physiol Imaging 7: 136-145, 1992.
110. van der Schaar PJ, Lamers CB, Masclee AA. The role of the barostat in human research and clinical practice. Scand J Gastroenterol Suppl 230: 52-63, 1999.
111. van der Veek PP, Steenvoorden M, Steens J, van der Schaar PJ, Brussee J, Masclee AA. Recto-colonic reflex is impaired in patients with irritable bowel syndrome. Neurogastroenterol Motil 19: 653-659, 2007.
112. van der Veek PP, Swenne CA, Vooren H, Schoneveld AL, Maestri R, Masclee AA. Viscerosensory-cardiovascular reflexes: altered baroreflex sensitivity in irritable bowel syndrome. Am J Physiol Regul Integr Comp Physiol 289: R970-R976, 2005.
113. van der Veek PP, Van Rood YR, Masclee AA. Symptom severity but not psychopathology predicts visceral hypersensitivity in irritable bowel syndrome. Clin Gastroenterol Hepatol 6: 321-328, 2008.
114. Wager TD, Rilling JK, Smith EE, Sokolik A, Casey KL, Davidson RJ, Kosslyn SM, Rose RM, Cohen JD. Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 303: 1162-1167, 2004.
115. White JC. Early studies have demonstrated that sensation of visceral distension was retained following extensive anterolateral chordotomy. Res Publ Assoc Res Nerv Ment Dis 23: 373-390, 1943.
116. Wilder-Smith CH. The balancing act: endogenous modulation of pain in functional gastrointestinal disorders. Gut 60: 1589-1599, 2011.
117. Williamson SJ, Lu ZL, Karron D, Kaufman L. Advantages and limitations of magnetic source imaging. Brain Topogr 4: 169-180, 1991.
118. Willis WD, Al-Chaer ED, Quast MJ, Westlund KN. A visceral pain pathway in the dorsal column of the spinal cord. Proc Natl Acad Sci USA 96: 7675-7679, 1999.
119. Willis WD, Westlund KN. Neuroanatomy of the pain system and of the pathways that modulate pain. J Clin Neurophysiol 14: 2-31, 1997.
120. Zuo XL, Li YQ, Huang KM, Kuang RG, Lv GP, Lu XF, Li JM, Desmond PV. Alterations in cerebral potentials evoked by rectal distention and drinking ice water in patients with irritable bowel syndrome. J Gastroenterol Hepatol 21: 1844-1849, 2006.